Characterization of TRPC2, an essential genetic component of VNS chemoreception, provides insights into the evolution of pheromonal olfaction in secondary-adapted marine mammals

Molecular Biology and Evolution

Volumn 27, Issue 7, 2010, Pages 1467-1477

  Yu, Li ^a   Jin, Wei ^a,b   Wang, Jia Xin ^a   Zhang, Xin ^a   Chen, Meng Meng ^a   Zhu, Zhou Hai ^a   Lee, Hang ^c   Lee, Muyeong ^c   Zhang, Ya Ping ^a,b  

^a YUNNAN UNIVERSITY   (China)

^b KUNMING INSTITUTE OF ZOOLOGY   (China)

^c Seoul National University   (South Korea)

Author keywords

Marine mammals; Pheromones; TRPC2; Vomeronasal system

Indexed keywords

PHEROMONE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 2; TRANSIENT RECEPTOR POTENTIAL CHANNEL C;

ANIMAL EXPERIMENT; AQUATIC ENVIRONMENT; ARTICLE; BIOINFORMATICS; CHEMORECEPTOR; CONTROLLED STUDY; EXON; GENE ISOLATION; GENETIC ANALYSIS; HABITAT; MARINE MAMMAL; MOLECULAR RECOGNITION; MUSTELIDAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRESSURE SENSATION; PSEUDOGENE; RIVER OTTER; SEAL; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SMELLING; VOMERONASAL ORGAN; AMINO ACID SEQUENCE; ANIMAL; CLASSIFICATION; EVOLUTION; GENETICS; GENOME; MAMMAL; MOLECULAR GENETICS; ODOR; PHYLOGENY; PHYSIOLOGY; SEQUENCE HOMOLOGY;

CETACEA; LUTRA CANADENSIS; MAMMALIA; PHOCA; ZALOPHUS;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; GENOME; MAMMALS; MOLECULAR SEQUENCE DATA; PHEROMONES; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; SMELL; TRPC CATION CHANNELS; VOMERONASAL ORGAN;

EID: 77953788899     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq027     Document Type: Article

References (84)

1. Arnason U, Xu X, Gullberg A, Graur D. 1996. The "Phoca standard: an external molecular reference for calibrating recent evolutionary divergences. J Mol Evol. 43:41-45.
2. Boehm U, Zou Z, Buck LB. 2005. Feedback loops link odor and pheromone signaling with reproduction. Cell 123:683-695.
3. Breathnach AS. 1960. The cetacean central nervous system. Biol Rev. 35:187-230.
4. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65:175-187.
5. Buck LB. 2000. The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611-618.
6. Caldwell DK, Caldwell MC. 1972. Senses and communication. In: Ridgway SH, editor. Mammals of the sea: biology and medicine. Springfield (IL): Charles C Thomas. p. 466-501.
7. Caldwell DK, Caldwell MC. 1977. Cetaceans. In: Sebeok TA, editor. How animals communicate. Bloomington (IN): Indiana University. p. 794-808.
8. Dixson AF. 1983. Observations on the evolution and behavioral significance of "sexual skin in female primates. Adv Study Behav. 13:63-106.
9. Dorries KM, Adkins-Regan E, Halpern BP. 1995. Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol Behav. 57:255-259.
10. Dudzinski KA. 2002. Communication. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego (CA): Academic Press. p. 248-268.
11. Dulac C. 1997. Molecular biology of pheromone perception in mammals. Semin Cell Dev Biol. 8:197-205. (Pubitemid 127348754)
12. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206.
13. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
14. Firestein S. 2001. How the olfactory system makes sense of scents. Nature 413:211-218.
15. Freitag J, Ludwig G, Andreini I, Rossler P, Breer H. 1998. Olfactory receptors in aquatic and terrestrial vertebrates. J Comp Physiol. 183:635-650.
16. Gatesy J. 2009. Whales and even-toed ungulates (Cetartiodactyla). In: Hedges SB, Kumar S, editors. Timetree of life. Oxford: Oxford University Press. p. 511-515.
17. Gittleman JL. 1991. Carnivore olfactory bulb size: allometry, phylogeny and ecology. J Zool. 225:253-272.
18. Grus WE, Shi P, Zhang YP, Zhang J. 2005. Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA. 102:5767-5772.
19. Grus WE, Shi P, Zhang J. 2007. Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol. 24:2153-2157.
20. Hadziselimović H, Dilberović F. 1977. The appearance of the otter brain. Acta Anat (Basel). 97:387-392.
21. Halpern M. 1987. The organization and function of the vomeronasal system. Annu Rev Neurosci. 10:325-362.
22. Hasegawa M, Thorne JL, Kishino H. 2003. Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution. Genes Genet Syst. 78:267-283.
23. Hassanin A, Douzery EJ. 2003. Molecular and morphological phylogenies of ruminantia and the alternative position of the moschidae. Syst Biol. 52:206-228.
24. Herrada G, Dulac C. 1997. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90: 763-773.
25. Hofmann T, Schaefer M, Schultz G, Gudermann T. 2000. Cloning, expression and subcellular localization of two novel splice variants of mouse transient receptor potential channel 2. Biochem J. 351:115-122.
26. Issel-Tarver L, Rine J. 1997. The evolution of mammalian olfactory receptor genes. Genetics 145:185-195.
27. Kaneko N, Debski EA, Wilson MC, Whitten WK. 1980. Puberty acceleration in mice. II. Evidence that the vomeronasal organ is a receptor for the primer pheromone in male mouse urine. Biol Reprod. 22:873-878.
28. Kelliher KR. 2007. The combined role of the main olfactory and vomeronasal systems in social communication in mammals. Horm Behav. 52:561-570.
29. Keverne EB. 1999. The vomeronasal organ. Science 286:716-720.
30. Kimchi T, Xu J, Dulac C. 2007. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448: 1009-1014.
31. Kishida T, Kubota S, Shirayama Y, Fukami H. 2007. The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans. Biol Lett. 3:428-430.
32. Koepfli KP, Deere KA, Slater GJ, Begg C, Begg K, Grassman L, Lucherini M, Veron G, Wayne RK. 2008. Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biol. 6:10.
33. Krettek A, Gullberg A, Arnason U. 1995. Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Lipotyphla. J Mol Evol. 41:952-957.
34. Kumar S, Dudley J, Nei M, Tamura K. 2008. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinformatics. 9:299-306.
35. Leypold BG, Yu CR, Leinders-Zufall MM, Kim T, Zufall F, Axel R. 2002. Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci USA. 99:637663-637681.
36. Li WH, Bousquet J. 1992. Relative-rate test for nucleotide substitutions between two lineages. Mol Biol Evol. 9:1185-1189.
37. Liman ER, Corey DP, Dulac C. 1999. TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci USA. 96:5791-5796.
38. Liman ER, Dulac C. 2006. TRPC2 and pheromone transduction. In: Heller S, Liedke W, editors. TRP ion channel function in sensory transduction and cellular signaling cascades. Boca Raton (FL): CRC Press LLC of Taylor and Francis Books, Inc. p. 1-30.
39. Liman ER, Innan H. 2003. Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA. 100:3328-3332.
40. Lloyd-Thomas A, Keverne EB. 1982. Role of the brain and accessory olfactory system in the block to pregnancy in mice. Neuroscience 7:907-913.
41. Lowell WR, Flanigan WF. 1980. Marine mammal chemo-reception. Mamm Rev. 10:53-59.
42. Mackay-Sim A, Duvall D, Graves BM. 1985. The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ. Brain Behav Evol. 27:186-194.
43. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell 96:713-723.
44. Mandiyan VS, Coats JK, Shah NM. 2005. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat Neurosci. 8:1660-1662.
45. Matsunami H, Buck LB. 1997. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775-784.
46. McClintock MK. 1984. Estrous synchrony: modulation of ovarian cycle length by female pheromones. Physiol Behav. 32:701-705.
47. Meisami E, Bhatnagar KP. 1998. Structure and diversity in mammalian accessory olfactory bulb. Microsc Res Tech. 43:476-499.
48. Miller EH. 2002. Territorial behavior. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego (CA): Academic Press. p. 1235-1243.
49. Morgane PJ, Jacobs MS. 1972. Comparative anatomy of the cetacean nervous system. In: Harrison RJ, editor. Functional anatomy of marine mammals. Vol.1. New York: Academic Press. p. 117-244.
50. Nef P, Hermans-Borgmeyer I, Artières-Pin H, Beasley L, Dionne VE, Heinemann SF. 1992. Spatial pattern of receptor expression in the olfactory epithelium. Proc Natl Acad Sci USA. 89:8948-8952.
51. Nei M, Niimura Y, Nozawa M. 2008. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet. 9:951-963.
52. Nikaido M, Matsuno F, Hamilton H, Brownell RL Jr., Cao Y, Ding W, Zuoyan Z, Shedlock AM, Fordyce RE, Hasegawa M, et al. 2001. Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA. 98:7384-7389.
53. Norris KS. 1991. Dolphin days: the life and times of the spinner dolphin. New York: W.W. Norton.
54. Oelschläger HA. 1989. Early development of the olfactory and terminalis system in baleen whales. Brain Behav Evol. 34:171-183.
55. Oelschläger HA, Buhl HE. 1985. Development and rudimentation of the peripheral olfactory system in the harbor porpoise Phocoena phocoena (Mammalia: Cetacea). J Morphol. 184: 351-360.
56. Oelschläger HA, Oelschläger JS. 2002. Brain. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego (CA): Academic Press. p. 133-158.
57. Pilleri G, Gihr M. 1970. The central nervous system of the mysticete and odontocete whale. Investig Cetacea (Berne). 2:87-135.
58. Restrepo D, Arellano J, Oliva AM, Schaefer ML, Lin W. 2004. Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice. Horm Behav. 46:247-256.
59. Ridgway S, Harrison R. 1981. Handbook of marine mammals. London: Academic Press.Vol. 1
60. Robinson-Rechavi M, Huchon D. 2000. RRTree: relative-rate tests between groups of sequences on a phylogenetic tree. Bio-informatics 16:296-297.
61. Ryba NJ, Tirindelli R. 1997. A new multigene family of putative pheromone receptors. Neuron 19:371-379.
62. Sam M, Vora S, Malnic B, Ma W, Novotny MV, Buck LB. 2001. Neuropharmacology. Odorants may arouse instinctive behaviours. Nature 412:142.
63. Schaal B, Coureaud G, Langlois D, Giniès C, Sémon E, Perrier G. 2003. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68-72.
64. Shi P, Zhang J. 2007. Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res. 17:166-174.
65. Stern K, McClintock MK. 1998. Regulation of ovulation by human pheromones. Nature 392:177-179.
66. Stowers L, Holy TE, Meister M, Dulac C, Koentges G. 2002. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493-1500.
67. Switzer RC, Johnson JJ, Kirsch JAW. 1980. Phylogeny through brain traits: relation of lateral olfactory tract fibers to the accessory olfactory formation as a palimpsest of mammalian descent. Brain Behav Evol. 17:339-363.
68. Swofford DL. 2001. PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4.0b8. Sunderland (MA): Sinauer Associates.
69. Taylor MA. 2002. Origins of marine mammals. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego (CA): Academic Press.
70. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The clustalx windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
71. Vannier B, Peyton M, Boulay G, Brown D, Qin N, Jiang M, Zhu X, BirnbaumerL.1999.Mouse trp2,thehomologueofthehumantrpc2 pseudogene, encodes mTrp2, a store depletion-activated capacita-tive Ca2\+ entry channel. Proc Natl Acad Sci USA. 96:2060-2064.
72. Webb DM, Cortés-Ortiz L, Zhang J. 2004. Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys. Mol Biol Evol. 21:697-704.
73. Wysocki CJ. 1979. Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci Biobehav Rev. 3:301-341.
74. Wysocki CJ, Lepri JJ. 1991. Consequences of removing the vomeronasal organ. J Steroid Biochem Mol Biol. 39:661-669.
75. Wysocki CJ, Meredith M. 1987. The vomeronasal system. In: Finger TE, Silver WL, editors. Neurobiology of taste and smell. New York: John Wiley. p. 125-150.
76. Xu F, Schaefer M, Kida I, Schafer J, Liu N, Rothman DL, Hyder F, Restrepo D, Shepherd GM. 2005. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Comp Neurol. 489:491-500.
77. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evolut. 15:568-573.
78. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
79. Yoon H, Enquist LW, Dulac C. 2005. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123:669-682.
80. Young JM, Kambere M, Trask BJ, Lane RP. 2005. Divergent V1R repertoires in five species: amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res. 15:231-240.
81. Young JM, Trask BJ. 2007. V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet. 23:212-215.
82. Zhang J, Nei M. 1997. Accuracies of ancestral amino acid sequences inferred by parsimony, likelihood, and distance methods. J Mol Evol. 44:S139-S146.
83. Zhang J, Webb DM. 2003. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA. 100:8337-8341.
84. Zufall F, Munger SD. 2001. From odor and pheromone transduction to the organization of the sense of smell. Trends Neurosci. 24:191-193.